St. Petersburg Homes with a Guest House For Sale

Looking for a new home with a guest house in St. Petersburg FL? If so, you're in the right place. It's here you'll be able to break down your search and browse property listings that fit all your needs and wants perfectly. As St. Petersburg's top hyper-local website for searching available homes with a guest house, our mission is to provide home buyers just like you an easy and effective way to find the perfect new place to live! If you register on our website, we can also send you disclosures, past sales history, dates and prices of homes recently sold nearby, and also all of the latest property listings that match your search criteria to hit the market, allowing you to stay one-step ahead of other St. Petersburg home buyers. 

To get your search started, simply start browsing all of the available St. Petersburg homes with a guest house below, and if you have any questions about a particular property or would even like to take that next step and schedule a home tour, call or text us at (813) 817-0345 now! 

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$11,500,000

1571 Oceanview Drive, ST PETERSBURG

7 Beds 11 Baths 12,046 SqFt Residential MLS® # TB8336934

$9,975,000

1956 Coffee Pot Boulevard Ne, ST PETERSBURG

4 Beds 6 Baths 6,605 SqFt Residential MLS® # TB8439235

$9,800,000

1075 31st Terrace Ne, ST PETERSBURG

5 Beds 8 Baths 6,800 SqFt Residential MLS® # TB8449312

$7,950,000

5237 61st Avenue S, ST PETERSBURG

4 Beds 5 Baths 4,511 SqFt Residential MLS® # TB8432616

$6,750,000

2807 Sunset Way, ST PETE BEACH

3 Beds 3 Baths 2,264 SqFt Residential MLS® # TB8445450

$6,400,000

↓ $400,000

2087 Michigan Avenue Ne, ST PETERSBURG

5 Beds 6 Baths 6,036 SqFt Residential MLS® # TB8386859

$6,000,000

5405 Leilani Drive, ST PETE BEACH

5 Beds 6 Baths 5,213 SqFt Residential MLS® # TB8418141

$5,995,000

6199 54th Street S, ST PETERSBURG

5 Beds 6 Baths 6,147 SqFt Residential MLS® # TB8439000

$5,950,000

↓ $200,000

1365 Brightwaters Boulevard Ne, ST PETERSBURG

5 Beds 5 Baths 6,060 SqFt Residential MLS® # TB8412312

$5,750,000

5845 Bahia Way S. Way W, ST PETE BEACH

4 Beds 5 Baths 5,009 SqFt Residential MLS® # L4956297

$5,350,000

↓ $600,000

1737 Brightwaters Boulevard Ne, ST PETERSBURG

4 Beds 7 Baths 7,710 SqFt Residential MLS® # TB8372318

$5,300,000

↓ $300,000

1210 Monterey Boulevard Ne, ST PETERSBURG

5 Beds 6 Baths 4,560 SqFt Residential MLS® # TB8417542

$5,099,000

↓ $101,000

504 55th Avenue, ST PETE BEACH

4 Beds 4 Baths 5,138 SqFt Residential MLS® # TB8442425

$4,995,000

838 Monterey Boulevard Ne, ST PETERSBURG

5 Beds 5 Baths 4,334 SqFt Residential MLS® # TB8452164

Openhouse

$4,995,000

↓ $155,000

2121 Bayou Grande Boulevard Ne, ST PETERSBURG

5 Beds 7 Baths 5,812 SqFt Residential MLS® # U8253104

Pending

$4,795,000

1761 Oceanview Drive, ST PETERSBURG

3 Beds 3 Baths 3,935 SqFt Residential MLS® # TB8422194

$4,600,000

↓ $150,000

2279 Mermaid Point Ne, ST PETERSBURG

5 Beds 5 Baths 4,814 SqFt Residential MLS® # TB8394418

$4,500,000

420 Coffee Pot Riviera Ne, ST PETERSBURG

5 Beds 5 Baths 5,144 SqFt Residential MLS® # U8248639

$4,500,000

1936 Carolina Avenue Ne, ST PETERSBURG

6 Beds 4 Baths 4,917 SqFt Residential MLS® # TB8435895

$4,495,000

↓ $500,000

801 Brightwaters Boulevard Ne, ST PETERSBURG

4 Beds 6 Baths 5,834 SqFt Residential MLS® # TB8430922

$4,450,000

1097 Eden Isle Drive Ne, ST PETERSBURG

5 Beds 5 Baths 6,015 SqFt Residential MLS® # TB8409397

$4,125,000

841 Ponce De Leon Drive, ST PETERSBURG

5 Beds 7 Baths 6,512 SqFt Residential MLS® # TB8392286

Openhouse

$3,959,000

↓ $291,000

103 5th Avenue N, ST PETERSBURG

5 Beds 7 Baths 6,617 SqFt Residential MLS® # TB8313332

$3,950,000

6627 Bayou Grande Boulevard Ne, ST PETERSBURG

4 Beds 4 Baths 4,028 SqFt Residential MLS® # U8235325

$3,899,000

↓ $51,000

1002 Pass A Grille Way, ST PETE BEACH

4 Beds 4 Baths 2,964 SqFt Residential MLS® # TB8420808

$3,730,000

↓ $20,000

7986 9th Avenue S, ST PETERSBURG

5 Beds 5 Baths 5,798 SqFt Residential MLS® # TB8353929

Openhouse

$3,499,000

107 10th Avenue, ST PETE BEACH

3 Beds 3 Baths 2,286 SqFt Residential MLS® # TB8428224

Pending

$3,495,000

924 42nd Avenue N, ST PETERSBURG

5 Beds 5 Baths 4,268 SqFt Residential MLS® # TB8392274

$3,295,000

↓ $155,000

4300 Bayshore Boulevard Ne, ST PETERSBURG

6 Beds 7 Baths 5,816 SqFt Residential MLS® # TB8436678

$3,275,000

3310 Sunset Drive N, ST PETERSBURG

3 Beds 4 Baths 4,577 SqFt Residential MLS® # O6304937

$3,100,000

255 46th Avenue, ST PETE BEACH

5 Beds 5 Baths 4,096 SqFt Residential MLS® # TB8441022

Pending

$3,049,000

↓ $200,000

526 16th Avenue Ne, ST PETERSBURG

4 Beds 4 Baths 3,584 SqFt Residential MLS® # TB8405897

$3,000,000

242 Estado Way Ne, ST PETERSBURG

5 Beds 5 Baths 3,680 SqFt Residential MLS® # TB8348460

Pending

$2,995,000

5820 Balao Way S, ST PETE BEACH

4 Beds 5 Baths 3,489 SqFt Residential MLS® # TB8446812

$2,995,000

↑ $45,000

935 Eden Isle Drive Ne, ST PETERSBURG

5 Beds 4 Baths 3,288 SqFt Residential MLS® # TB8371186

$2,990,000

310 8th Avenue N, ST PETERSBURG

4 Beds 5 Baths 4,082 SqFt Residential MLS® # TB8340465

$2,975,000

297 1st Street W, ST PETERSBURG

4 Beds 2 Baths 3,323 SqFt Residential MLS® # TB8447039

$2,950,000

970 Boca Ciega Isle Drive, ST PETE BEACH

4 Beds 3 Baths 3,185 SqFt Residential MLS® # A4668251

Pending

$2,800,000

2501 Sunrise Drive Se, ST PETERSBURG

3 Beds 4 Baths 2,824 SqFt Residential MLS® # TB8434280

$2,795,000

485 Rafael Boulevard Ne, ST PETERSBURG

5 Beds 6 Baths 4,280 SqFt Residential MLS® # TB8430112

$2,750,000

720 16th Avenue Ne, ST PETERSBURG

4 Beds 5 Baths 3,220 SqFt Residential MLS® # TB8434867

$2,699,999

↓ $100,000

4913 58th Avenue S, ST PETERSBURG

4 Beds 4 Baths 3,620 SqFt Residential MLS® # TB8439549

$2,675,000

↓ $125,000

422 55th Avenue, ST PETE BEACH

5 Beds 4 Baths 2,993 SqFt Residential MLS® # TB8412746

$2,670,000

↓ $76,650

220 90th Avenue Ne, ST PETERSBURG

4 Beds 4 Baths 3,673 SqFt Residential MLS® # TB8423274

$2,650,000

4959 58th Avenue S, ST PETERSBURG

4 Beds 3 Baths 3,154 SqFt Residential MLS® # TB8439046

Openhouse

$2,595,000

323 Appian Way Ne, ST PETERSBURG

5 Beds 5 Baths 3,653 SqFt Residential MLS® # TB8343227

$2,595,000

↓ $100,000

339 55th Avenue, ST PETE BEACH

5 Beds 4 Baths 3,028 SqFt Residential MLS® # TB8425322

$2,590,000

1818 Dolphin Boulevard S, ST PETERSBURG

4 Beds 3 Baths 2,420 SqFt Residential MLS® # TB8344834

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Continue Searching Homes with a Guest House in Florida 

Not seeing the right home with a guest house that fits your needs, wants, or budget here? Continue searching homes for sale with a guest house for sale in other Florida cities and towns using our homes with a guest house-by-city directory below. 

Buying a Home with a Guest House in St. Petersburg, FL  

St. Petersburg, FL, known for its stunning waterfronts and thriving arts community, is quickly becoming a top destination for homebuyers seeking properties with guest houses. The growing popularity of homes with additional living spaces in this vibrant city reflects modern trends in home functionality, while also taking advantage of its unique local appeal.

Why Guest Houses Are Gaining Popularity  

Homes with guest houses offer unmatched versatility. They provide extra space for accommodating family members, particularly for multi-generational households. This is especially attractive in St. Petersburg, where the warm climate and picturesque surroundings draw many retirees eager to be close to loved ones. Guest houses also offer privacy for visitors, enhancing their stay in this bustling yet scenic city.  

Another key driver is the potential for rental income. St. Petersburg, with its world-class beaches, renowned museums such as The Dalí, and lively events like the Saturday Morning Market, attracts a steady stream of tourists year-round. Properties with guest houses can be ideal for short-term rentals, giving homeowners the opportunity to generate income while leveraging the city’s booming tourism industry.  

St. Petersburg-Specific Appeal  

With its warm, sunny weather and pedestrian-friendly neighborhoods, St. Petersburg provides an ideal backdrop for properties with guest houses. Many of these homes are located in charming areas near attractions like the Central Arts District or along the waterfront, where guest houses are especially sought-after for their potential to accommodate both locals and visitors. Additionally, as the city sees an influx of people relocating from northern states, buyers are actively seeking residences that blend practicality with Florida’s renowned laid-back lifestyle.  

Buying a home with a guest house in St. Petersburg is more than a real estate purchase—it’s an investment in flexibility, lifestyle, and future earning potential, all set against the backdrop of one of Florida’s most exciting and culture-filled cities. 

St. Petersburg Realtors Specializing in Homes With a Guest House

If you are thinking about buying or selling a home in St. Petersburg with a guest house, our team can help you navigate the current housing landscape and get you the best possible price based on current market conditions. Simply put, we know the St. Petersburg real estate market better than anyone!

Contact Mike + Michelle to see why our expertise working with St. Petersburg homes with a guest house helps makes us the perfect fit for all your home buying and selling needs. And in the meantime, also continue searching other homes for sale in the area using our Advanced Search.